Striatal action-value neurons reconsidered

  1. Lotem Elber-Dorozko  Is a corresponding author
  2. Yonatan Loewenstein
  1. Hebrew University of Jerusalem, Israel

Abstract

It is generally believed that during economic decisions, striatal neurons represent the values associated with different actions. This hypothesis is based on studies, in which the activity of striatal neurons was measured while the subject was learning to prefer the more rewarding action. Here we show that these publications are subject to at least one of two critical confounds. First, we show that even weak temporal correlations in the neuronal data may result in an erroneous identification of action-value representations. Second, we show that experiments and analyses designed to dissociate action-value representation from the representation of other decision variables cannot do so. We suggest solutions to identifying action-value representation that are not subject to these confounds. Applying one solution to previously identified action-value neurons in the basal ganglia we fail to detect action-value representations. We conclude that the claim that striatal neurons encode action-values must await new experiments and analyses.

Data availability

The data of the basal ganglia recordings from (Ito and Doya 2009) is available online at https://groups.oist.jp/ncu/data and was analyzed with permission from the authors. Motor cortex data (recorded by Oren Peles in Eilon Vaadia's lab) and auditory cortex data (taken from the recordings in (Hershenhoren, Taaseh, Antunes, & Nelken, 2014)) is available at https://github.com/lotem-elber/striatal-action-value-neurons-reconsidered-codes (Elber-Dorozko & Loewenstein 2018). The custom MATLAB scripts used to create simulated neurons and to analyze simulated and recorded neurons are also available at https://github.com/lotem-elber/striatal-action-value-neurons-reconsidered-codes.

The following previously published data sets were used

Article and author information

Author details

  1. Lotem Elber-Dorozko

    The Edmond and Lily Safra Center for Brain Sciences, Hebrew University of Jerusalem, Jerusalem, Israel
    For correspondence
    lotem.elber@mail.huji.ac.il
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1235-8651
  2. Yonatan Loewenstein

    The Edmond and Lily Safra Center for Brain Sciences, Hebrew University of Jerusalem, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.

Funding

Israel Science Foundation (757/16)

  • Yonatan Loewenstein

Deutsche Forschungsgemeinschaft (CRC1080)

  • Yonatan Loewenstein

Gatsby Charitable Foundation

  • Yonatan Loewenstein

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Timothy E Behrens, University of Oxford, United Kingdom

Version history

  1. Received: December 11, 2017
  2. Accepted: May 13, 2018
  3. Accepted Manuscript published: May 31, 2018 (version 1)
  4. Version of Record published: June 19, 2018 (version 2)

Copyright

© 2018, Elber-Dorozko & Loewenstein

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 4,464
    views
  • 657
    downloads
  • 21
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Lotem Elber-Dorozko
  2. Yonatan Loewenstein
(2018)
Striatal action-value neurons reconsidered
eLife 7:e34248.
https://doi.org/10.7554/eLife.34248

Share this article

https://doi.org/10.7554/eLife.34248

Further reading

    1. Neuroscience
    Songyao Zhang, Tuo Zhang ... Tianming Liu
    Research Article

    Cortical folding is an important feature of primate brains that plays a crucial role in various cognitive and behavioral processes. Extensive research has revealed both similarities and differences in folding morphology and brain function among primates including macaque and human. The folding morphology is the basis of brain function, making cross-species studies on folding morphology important for understanding brain function and species evolution. However, prior studies on cross-species folding morphology mainly focused on partial regions of the cortex instead of the entire brain. Previously, our research defined a whole-brain landmark based on folding morphology: the gyral peak. It was found to exist stably across individuals and ages in both human and macaque brains. Shared and unique gyral peaks in human and macaque are identified in this study, and their similarities and differences in spatial distribution, anatomical morphology, and functional connectivity were also dicussed.

    1. Neuroscience
    Avani Koparkar, Timothy L Warren ... Lena Veit
    Research Article

    Complex skills like speech and dance are composed of ordered sequences of simpler elements, but the neuronal basis for the syntactic ordering of actions is poorly understood. Birdsong is a learned vocal behavior composed of syntactically ordered syllables, controlled in part by the songbird premotor nucleus HVC (proper name). Here, we test whether one of HVC’s recurrent inputs, mMAN (medial magnocellular nucleus of the anterior nidopallium), contributes to sequencing in adult male Bengalese finches (Lonchura striata domestica). Bengalese finch song includes several patterns: (1) chunks, comprising stereotyped syllable sequences; (2) branch points, where a given syllable can be followed probabilistically by multiple syllables; and (3) repeat phrases, where individual syllables are repeated variable numbers of times. We found that following bilateral lesions of mMAN, acoustic structure of syllables remained largely intact, but sequencing became more variable, as evidenced by ‘breaks’ in previously stereotyped chunks, increased uncertainty at branch points, and increased variability in repeat numbers. Our results show that mMAN contributes to the variable sequencing of vocal elements in Bengalese finch song and demonstrate the influence of recurrent projections to HVC. Furthermore, they highlight the utility of species with complex syntax in investigating neuronal control of ordered sequences.